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Tumor Microenvironment and Immunobiology

Omega-3 Eicosapentaenoic Acid Reduces Prostate Tumor Vascularity

Nikunj Gevariya, Gabriel Lachance, Karine Robitaille, Charles Joly Beauparlant, Lisanne Beaudoin, Éric Fournier, Yves Fradet, Arnaud Droit, Pierre Julien, André Marette, Alain Bergeron and Vincent Fradet
Nikunj Gevariya
1Laboratoire d'Uro-Oncologie Expérimentale, Oncology Axis, Centre de recherche du CHU de Québec-Université Laval, Québec, Québec, Canada.
2Centre de Recherche sur le Cancer de l’Université Laval, Québec, Québec, Canada.
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  • ORCID record for Nikunj Gevariya
Gabriel Lachance
1Laboratoire d'Uro-Oncologie Expérimentale, Oncology Axis, Centre de recherche du CHU de Québec-Université Laval, Québec, Québec, Canada.
2Centre de Recherche sur le Cancer de l’Université Laval, Québec, Québec, Canada.
3Centre de recherche de l’IUCPQ, Québec, Québec, Canada.
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Karine Robitaille
1Laboratoire d'Uro-Oncologie Expérimentale, Oncology Axis, Centre de recherche du CHU de Québec-Université Laval, Québec, Québec, Canada.
2Centre de Recherche sur le Cancer de l’Université Laval, Québec, Québec, Canada.
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Charles Joly Beauparlant
4Endocrinology and Nephrology Axis, Centre de recherche du CHU de Québec-Université Laval, Québec, Québec, Canada.
5Laboratoire de bio-informatique and Centre de Génomique du Centre de recherche du CHU de Québec-Université Laval, Québec, Québec, Canada.
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Lisanne Beaudoin
1Laboratoire d'Uro-Oncologie Expérimentale, Oncology Axis, Centre de recherche du CHU de Québec-Université Laval, Québec, Québec, Canada.
2Centre de Recherche sur le Cancer de l’Université Laval, Québec, Québec, Canada.
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Éric Fournier
2Centre de Recherche sur le Cancer de l’Université Laval, Québec, Québec, Canada.
4Endocrinology and Nephrology Axis, Centre de recherche du CHU de Québec-Université Laval, Québec, Québec, Canada.
5Laboratoire de bio-informatique and Centre de Génomique du Centre de recherche du CHU de Québec-Université Laval, Québec, Québec, Canada.
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Yves Fradet
1Laboratoire d'Uro-Oncologie Expérimentale, Oncology Axis, Centre de recherche du CHU de Québec-Université Laval, Québec, Québec, Canada.
2Centre de Recherche sur le Cancer de l’Université Laval, Québec, Québec, Canada.
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  • ORCID record for Yves Fradet
Arnaud Droit
4Endocrinology and Nephrology Axis, Centre de recherche du CHU de Québec-Université Laval, Québec, Québec, Canada.
5Laboratoire de bio-informatique and Centre de Génomique du Centre de recherche du CHU de Québec-Université Laval, Québec, Québec, Canada.
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Pierre Julien
4Endocrinology and Nephrology Axis, Centre de recherche du CHU de Québec-Université Laval, Québec, Québec, Canada.
6Centre de recherche en endocrinologie, métabolisme et inflammation de l’Université Laval, Québec, Québec, Canada.
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André Marette
3Centre de recherche de l’IUCPQ, Québec, Québec, Canada.
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Alain Bergeron
1Laboratoire d'Uro-Oncologie Expérimentale, Oncology Axis, Centre de recherche du CHU de Québec-Université Laval, Québec, Québec, Canada.
2Centre de Recherche sur le Cancer de l’Université Laval, Québec, Québec, Canada.
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Vincent Fradet
1Laboratoire d'Uro-Oncologie Expérimentale, Oncology Axis, Centre de recherche du CHU de Québec-Université Laval, Québec, Québec, Canada.
2Centre de Recherche sur le Cancer de l’Université Laval, Québec, Québec, Canada.
7Centre nutrition, santé et société (NUTRISS) et Institut sur la nutrition et les aliments fonctionnels (INAF), Québec, Québec, Canada.
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  • For correspondence: vincent.fradet@fmed.ulaval.ca
DOI: 10.1158/1541-7786.MCR-20-0316
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Abstract

The impact of omega (ω)-3 fatty acids on prostate cancer is controversial in epidemiological studies but experimental studies suggest a protective effect. However, little is known about the mechanism of action. Here, we studied the effects of purified fatty acid molecules on prostate tumor progression using the TRAMP-C2 syngeneic immunocompetent mouse model. Compared with ω-6 or ω-9–supplemented animals, we observed that late-stage prostate tumor growth was reduced with a monoacylglyceride (MAG)-conjugated form of eicosapentaenoic acid (EPA) supplementation, whereas docosahexanenoic acid (DHA) caused an early reduction. MAG–EPA significantly decreased tumor blood vessel diameter (P < 0.001). RNA sequencing analysis revealed that MAG–EPA downregulated angiogenesis- and vascular-related pathways in tumors. We also observed this tissue vascular phenotype in a clinical trial testing MAG–EPA versus a high oleic sunflower oil placebo. Using anti-CD31 IHC, we observed that MAG–EPA reduced blood vessel diameter in prostate tumor tissue (P = 0.03) but not in normal adjacent tissue. Finally, testing autocrine and paracrine effects in an avascular tumor spheroid growth assay, both exogenous MAG–EPA and endogenous ω3 reduced VEGF secretion and in vitro endothelial cell tube formation and blocked tumor spheroid growth, suggesting that ω3 molecules can directly hinder prostate cancer cell growth. Altogether, our results suggest that fatty acids regulate prostate cancer growth and that a tumor-specific microenvironment is required for the anti-vascular effect of MAG–EPA in patients with prostate cancer.

Implications: Increasing the amount of ingested EPA omega-3 subtype for patients with prostate cancer might help to reduce prostate tumor progression by reducing tumor vascularization.

Footnotes

  • Note: Supplementary data for this article are available at Molecular Cancer Research Online (http://mcr.aacrjournals.org/).

  • Mol Cancer Res 2021;XX:XX–XX

  • Received April 7, 2020.
  • Revision received July 31, 2020.
  • Accepted November 25, 2020.
  • Published first December 1, 2020.
  • ©2020 American Association for Cancer Research.

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This OnlineFirst version was published on January 14, 2021
doi: 10.1158/1541-7786.MCR-20-0316

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Omega-3 Eicosapentaenoic Acid Reduces Prostate Tumor Vascularity
Nikunj Gevariya, Gabriel Lachance, Karine Robitaille, Charles Joly Beauparlant, Lisanne Beaudoin, Éric Fournier, Yves Fradet, Arnaud Droit, Pierre Julien, André Marette, Alain Bergeron and Vincent Fradet
Mol Cancer Res January 14 2021 DOI: 10.1158/1541-7786.MCR-20-0316

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Omega-3 Eicosapentaenoic Acid Reduces Prostate Tumor Vascularity
Nikunj Gevariya, Gabriel Lachance, Karine Robitaille, Charles Joly Beauparlant, Lisanne Beaudoin, Éric Fournier, Yves Fradet, Arnaud Droit, Pierre Julien, André Marette, Alain Bergeron and Vincent Fradet
Mol Cancer Res January 14 2021 DOI: 10.1158/1541-7786.MCR-20-0316
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Molecular Cancer Research
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